Abstract
This article is a response to Vibranovski et al.See correspondence article http://www.biomedcentral.com/1741-7007/10/49 and the original research article http://www.biomedcentral.com/1741-7007/9/29We have previously reported a high propensity of testis-expressed X-linked genes to activation in meiotic cells, a similarity in global gene expression between the X chromosome and autosomes in meiotic germline, and under-representation of various types of tissue-specific genes on the X chromosome. Based on our findings and a critical review of the current literature, we believe that there is no global and severe silencing of the X chromosome in the meiotic male germline of Drosophila. The term 'meiotic sex chromosome inactivation' (MSCI) therefore seems misleading when used to describe the minor underexpression of the X chromosome in the testis of Drosophila, because this term erroneously implies a profound and widespread silencing of the X-linked genes, by analogy to the well-studied MSCI system in mammals, and therefore distracts from identification and analysis of the real mechanisms that orchestrate gene expression and evolution in this species.
Highlights
Introduction meiotic sex chromosome inactivation (MSCI) has been convincingly documented in mammals, and its presence in other taxa has often been inferred based on several lines of evidence [1], the widespread conservation of this phenomenon has been questioned by several recent studies, including ours, that have shown little evidence for meiotic sex chromosome inactivation’ (MSCI) in birds [2] and flies [3,4]
Our analysis of the gene expression in the Drosophila male germline [3] has shown that in this species, the X-linked and autosomal genes have a similar propensity to activation in meiotic cells, and that the average gene expression in meiotic germline is similar between X chromosome and autosomes
Concluded that a global meiotic sex-chromosome inactivation does not occur in Drosophila, and that other mechanisms such as specific chromatin modifications are more likely explanations for the paucity of the tissue-specific genes on the Drosophila X chromosome. These conclusions were questioned by Vibranovski et al who suggested that 1) our choice of the normalizing ‘housekeeping’ control undermined our analysis of the propensity of the X-linked genes to activation in the meiotic germline, 2) small but significant underexpression of the X chromosome in testis tissue can be identified in our microarray data, and 3) under-representation of the tissue-specific genes on the X chromosome is not supported by statistical analysis
Summary
Meiotic sex chromosome inactivation (MSCI) has been convincingly documented in mammals, and its presence in other taxa has often been inferred based on several lines of evidence [1], the widespread conservation of this phenomenon has been questioned by several recent studies, including ours, that have shown little evidence for MSCI in birds [2] and flies [3,4]. Meiklejohn et al recently showed that, regardless of the experimental model or of the high-throughput method used in previous studies [4,9,10], the global underexpression of the X chromosome compared with the autosomes in the Drosophila meiotic male germline was 33% at most This is in striking contrast to the magnitude of changes in mammals expected from the high frequency and severity of the Xlinked gene silencing in MSCI [5], and confirmed by the eightfold reduction in mammalian X-chromosome expression in the testis [11]. Our hypothesis that the X chromosome provides an inferior environment for diverse types of tissue-specialized genes gains further support
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