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Genes versus chromosomes: A battle for expression in fly testes

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Unique sex chromosomes occur in species from humans to birds, worms, and flies. An unequal pair of sex chromosomes, each carrying a different complement of genes, requires specific efforts to regulate and balance the expression of sex-chromosomal genes. Like mammals, the fruit fly Drosophila has two different sex chromosomes, with XX females and XY males. A study published on July 12th in PLOS Biology shows that in the Drosophila testes–where unique X sperm and Y sperm are generated–multiple mechanisms vie to regulate expression of genes from the single X chromosome, and these bear witness to an ancient evolutionary struggle for control.

In mammals, a process called meiotic sex chromosome inactivation (MSCI) silences most of the genes on the X and Y sex chromosomes during sperm development. Male mice with defects in MSCI are infertile, suggesting that MSCI is essential for the generation of sperm cells, at least in mice. In Drosophila, there has been no conclusive evidence for the existence of MSCI. But like their mammalian counterparts, fruit fly males presumably need to regulate sex chromosomal gene expression in their testes.

Emily Landeen, from the University of Rochester, USA, and colleagues study gene expression in the germ line (i.e., the testes) of Drosophila males. In previous studies, researchers had created fly strains with random insertions of synthetic genes whose expression can be easily visualized. When these so-called transgenes landed on an autosome (any non-sex chromosome), they were expressed strongly in the testes. However, when the transgene insertions were on the X chromosome, expression in the testes was several-fold weaker.

Based on these results, the researchers concluded that a novel form of sex chromosome-specific transcriptional suppression occurs in Drosophila testes. In this study, they characterize this transcriptional suppression of X-chromosomal genes in detail and explore its evolutionary consequences.

Using experimental fly strains with well-characterized abnormal chromosome constellations (some specifically engineered to move genes normally found on the X to an autosome and vice versa), the researchers found that most genes that originate from the X are transcriptionally suppressed several-fold. Such genes show two- to four-fold higher expression when moved from the repressive environment of the X chromosome to the more permissive environment of the autosomes. Paradoxically, despite the strong transcriptional repression of the X chromosome revealed in the experimental fly strains, X-linked gene expression does not appear repressed in the testes of normal fly strains.

One possible explanation is that promoters, which regulate gene expression, have adapted to overcome the repressive X chromosome environment in the testes. To test this, the researchers performed a computer-based analysis of the DNA sequences in putative promoter regions of testis-expressed genes. Among these, they looked specifically for sequence motifs that are over-represented on the X chromosome compared with autosomes.

The analysis indeed identified several candidate promoter motifs. For one of them, the researchers were able to confirm experimentally that this short stretch of DNA, when placed upstream of a reporter gene on the X chromosome, triggers strong expression in the testes. In other words, if the motif is present upstream of a gene on the X, that gene can overcome X suppression.

The researchers conclude that their findings "show that the expression of X-linked genes in the Drosophila testes reflects a balance between chromosome-wide transcriptional suppression and the long-term compensatory evolution by sex-linked genes which have recruited strong promoters". Discussing why X suppression might have evolved only for its effects to be cancelled by the adaptation of strong promoters, they suggest that "X suppression may have evolved deep in the past for reasons that no longer hold"– perhaps as an analog of MSCI– "and, since then, strong promoters have evolved en masse to compensate".

In any case, the researchers state that "the constrained transcriptional environment of the X chromosome in the testes has consequences for gene expression and genome evolution". One example they mention (and for which they have some experimental support) is that "X suppression […] may impose an upper limit on the expression level achievable in the testes". "This", they say, "may help to explain why many parent genes on the X chromosome have spawned testes-expressed duplicate genes on the autosomes", namely as "a complementary means to boost expression and compensate for X suppression".

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In your coverage please use this URL to provide access to the freely available article in PLOS Biology: http://dx.plos.org/10.1371/journal.pbio.1002499

Citation: Landeen EL, Muirhead CA, Wright L, Meiklejohn CD, Presgraves DC (2016) Sex Chromosome-wide Transcriptional Suppression and Compensatory Cis-Regulatory Evolution Mediate Gene Expression in the Drosophila Male Germline. PLoS Biol 14(7): e1002499. doi:10.1371/journal.pbio.1002499

Funding: DCP was supported by grant no. 000596 from the David and Lucile Packard Foundation (http://www.packard.org), grant no. BR-5006 from the Alfred P. Sloan Foundation (http://www.sloan.org), and funds from the University of Rochester. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Competing Interests: The authors have declared that no competing interests exist.

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Emily Landeen
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