Transcriptome profiling of Nasonia vitripennis testis reveals novel transcripts expressed from the selfish B chromosome, paternal sex ratio

Abstract

A widespread phenomenon in nature is sex ratio distortion of arthropod populations caused by microbial and genetic parasites. Currently little is known about how these agents alter host developmental processes to favor one sex or the other. The paternal sex ratio (PSR) chromosome is a nonessential, paternally transmitted centric fragment that segregates in natural populations of the jewel wasp, Nasonia vitripennis. To persist, PSR is thought to modify the hereditary material of the developing sperm, with the result that all nuclear DNA other than the PSR chromosome is destroyed shortly after fertilization. This results in the conversion of a fertilized embryo--normally a female--into a male, thereby insuring transmission of the "selfish" PSR chromosome, and simultaneously leading to wasp populations that are male-biased. To begin to understand this system at the mechanistic level, we carried out transcriptional profiling of testis from WT and PSR-carrying males. We identified a number of transcripts that are differentially expressed between these conditions. We also discovered nine transcripts that are uniquely expressed from the PSR chromosome. Four of these PSR-specific transcripts encode putative proteins, whereas the others have very short open reading frames and no homology to known proteins, suggesting that they are long noncoding RNAs. We propose several different models for how these transcripts could facilitate PSR-dependent effects. Our analyses also revealed 15.71 MB of novel transcribed regions in the N. vitripennis genome, thus increasing the current annotation of total transcribed regions by 53.4%. Finally, we detected expression of multiple meiosis-related genes in the wasp testis, despite the lack of conventional meiosis in the male sex.

Figure 1

Chromosomal locations of PSR-specific and normal chromosome transcripts obtained from RNA-seq by using DNA fluorescence in situ hybridization. (A−C) Three probes, each corresponding to one of three transcripts (names, respectively) present only in the PSR+ testis, localize specifically to the PSR chromosome (red regions, indicated by red arrows). (D, E) Probes corresponding to two different transcripts present in both control and PSR+ testes highlight single regions on a single normal chromosome.

Figure 2

Scatter plot of PSR vs. WT testes with coefficient of determination. Scatter plot of fragments per kilobase of exon per million fragments mapped values for genes and NTRs comparing expression values for PSR (Y-axis) and WT (X-axis) testes. The coefficient of determination (R²) is displayed in top left.

Figure 3

Model for initial alteration of the paternal genome by PSR as suggested by testis transcriptome profiling. PSR-specific transcripts are expressed during spermatogenesis. These transcripts or their encoded proteins facilitate an unknown modification of the paternal chromatin that disrupts its normal behavior during the first mitotic division of the embryo. PSR, however, spares itself this fate and is transmitted with the viable maternal set. The paternal set is lost, converting what should become a diploid female embryo into a haploid male, the PSR-transmitting sex.