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Open Access Correspondence

Re-analysis of the larval testis data on meiotic sex chromosome inactivation revealed evidence for tissue-specific gene expression related to the drosophila X chromosome

Maria D Vibranovski1*, Yong E Zhang12, Claus Kemkemer1, Hedibert F Lopes3, Timothy L Karr4 and Manyuan Long1*

Author affiliations

1 Department of Ecology and Evolution, The University of Chicago, 1101 East 57th Street, Chicago, IL 60637, USA

2 Key Laboratory of the Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beichen West Road, Chaoyang District, Beijing 100101, PR China

3 The University of Chicago Booth School of Business, 5807 South Woodlawn Ave., Chicago, IL 60637, USA

4 Center for Evolutionary Medicine and Informatics and Center for Infectious Diseases and Vaccinology, The Biodesign Institute, Arizona State University, 1001 South McAllister Ave., Tempe, AZ 85287, USA

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Citation and License

BMC Biology 2012, 10:49  doi:10.1186/1741-7007-10-49

Published: 12 June 2012

Abstract

Background

Meiotic sex chromosome inactivation (MSCI) during spermatogenesis has been proposed as one of the evolutionary driving forces behind both the under-representation of male-biased genes on, and the gene movement out of, the X chromosome in Drosophila. However, the relevance of MSCI in shaping sex chromosome evolution is controversial. Here we examine two aspects of a recent study on testis gene expression (Mikhaylova and Nurminsky, BMC Biol 2011, 9:29) that failed to support the MSCI in Drosophila. First, Mikhaylova and Nurminsky found no differences between X-linked and autosomal genes based on the transcriptional profiling of the early testis development, and thus concluded that MSCI does not occur in D. melanogaster. Second, they also analyzed expression data from several D. melanogaster tissues and concluded that under-representation on the X chromosome is not an exclusive property of testis-biased genes, but instead, a general property of tissue-specific genes.

Results

By re-analyzing the Mikhaylova and Nurminsky's testis data and the expression data on several D. melanogaster tissues, we made two major findings that refuted their original claims. First, the developmental testis data has generally greater experimental error than conventional analyses, which reduced significantly the power to detect chromosomal differences in expression. Nevertheless, our re-analysis observed significantly lower expression of the X chromosome in the genomic transcriptomes of later development stages of the testis, which is consistent with the MSCI hypothesis. Second, tissue-specific genes are also in general enriched with genes more expressed in testes than in ovaries, that is testis-biased genes. By completely excluding from the analyses the testis-biased genes, which are known to be under-represented in the X, we found that all the other tissue-specific genes are randomly distributed between the X chromosome and the autosomes.

Conclusions

Our findings negate the original study of Mikhaylova and Nurminsky, which concluded a lack of MSCI and generalized the pattern of paucity in the X chromosome for tissue-specific genes in Drosophila. Therefore, MSCI and other selection-based models such as sexual antagonism, dosage compensation, and meiotic-drive continue to be viable models as driving forces shaping the genomic distribution of male-related genes in Drosophila.