The silkworm Z chromosome is enriched in testis-specific genes

Abstract

The role of sex chromosomes in sex determination has been well studied in diverse groups of organisms. However, the role of the genes on the sex chromosomes in conferring sexual dimorphism is still being experimentally evaluated. An unequal complement of sex chromosomes between two sexes makes them amenable to sex-specific evolutionary forces. Sex-linked genes preferentially expressed in one sex over the other offer a potential means of addressing the role of sex chromosomes in sexual dimorphism. We examined the testis transcriptome of the silkworm, Bombyx mori, which has a ZW chromosome constitution in the female and ZZ in the male, and show that the Z chromosome harbors a significantly higher number of genes expressed preferentially in testis compared to the autosomes. We hypothesize that sexual antagonism and absence of dosage compensation have possibly led to the accumulation of many male-specific genes on the Z chromosome. Further, our analysis of testis-specific paralogous genes suggests that the accumulation on the Z chromosome of genes advantageous to males has occurred primarily by translocation or tandem duplication.

Figure 1.—

RT–PCR analysis of expression of 15 predicted testis-specific genes. β-Actin was used as an internal control. Details of accession numbers and tissue specificity as predicted in silico are given in Table S3. Primer sequences are given in Table S2.

Figure 2.—

Distribution of testis-specific genes identified through microarray analysis (top panel) and through EST and fl-DNA sequence analysis (bottom panel) on different chromosomes of B. mori. There is a significant difference (P < 0.001) between the number of testis-specific genes present on the Z chromosome and on autosomes in both the cases. Among 1104 microarray-validated testis-specific genes, 1029 were successfully mapped onto B. mori chromosomes. The average number of testis-specific genes on autosomes was calculated to be 35 ± 2, which is indicated by a black horizontal line on the histogram. Of 1984 testis-specific genes identified through analysis of testis-derived fl-cDNAs and ESTs, 1857 genes could be mapped onto B. mori chromosomes. The average number of genes on autosomes was calculated to be 63 ± 4 (green horizontal line).

Figure 3.—

Distribution of tissue-specific genes (excluding testis and ovary) on different chromosomes of B. mori. Of 501 other tissue-specific genes, 465 were successfully mapped. The average number of other tissue-specific genes on autosomes was calculated to be 16, which is indicated by the black horizontal line on the histogram.

Figure 4.—

Physical map showing the distribution of 1029 microarray-validated testis-specific genes on B. mori chromosomes.