Theories of sex chromosome evolution generally suppose that the X and Y chromosomes evolved from a homologous pair, with a proto-Y having "degenerated" into its present-day heterochromatic form (e.g., ref. 133). The D. melanogaster Y chromosome carries male-fertility factors but has no essential genes apart from the NOR (or bobbed locus), which is duplicated on the X. This explains why X/0 males are viable but sterile. Brosseau in 1960 (134) described seven Y-linked fertility factors. However, that number was reduced to six in 1981 when the existence of one of Brosseau's genes could not be confirmed (135-137); they are kl-1, kl-2, kl-3 and kl-5 on Yl, and ks-1 and ks-2 on YS, where k refers to a male-fertility complex (138). At least three of these genes are extremely large, approx 1.3-4.3 Mb. kl-3, kl-5 and ks-1 are associated with megabase-size lampbrushlike loops visible in primary spermatocyte nuclei (139), and kl-5 contains a "mega-intron" composed of repetitive DNAs (140). Such large introns may be a normal structural feature of single-copy genes in heterochromatin because both the rolled gene in chromosome 2 heterochromatin (141) and the Parp gene in chromosome 3 heterochromatin (67) are known to have large introns composed of repetitive DNAs.
Using a new approach to scrutinize unmapped sequences in the Drosophila genome databases, Carvalho and colleagues recently discovered four, and possibly six, additional Y-linked genes (142,143). Moreover, they speculate that as many as 10 more genes may yet be found. kl-2, kl-3 and kl-5 all encode previously identified sperm axonemal dynein components (144,145), and ks-1 and ks-2 may correspond to the newly discovered genes ORYand CCY, respectively, both of which encode proteins with coiled-coil motifs. Three other new genes encode protein phosphatases of unknown function, and the PRY product may be involved in sperm-egg recognition (143). A sequence corresponding to kl-1 still awaits identification. As pointed out by Carvalho et al. (143), a striking feature of nearly all of these genes is that their closest homologs are autosomal rather than X linked. This suggests that the ancestral Y genes originated on the autosomes and were translocated somehow to the proto-Y. Models of Y evolution certainly allow for such gene transposition, but the apparent large contribution of genes from the autosomes (as opposed to the X) is curious. For a discussion of these and other interesting aspects of Y chromosome evolution, see ref. 143.
Chromosome 4 is an unusual autosome in many respects (e.g., see refs. 146,147). At only approx 5 Mb, it is obviously much smaller than chromosome 2 or 3 (see Fig. 1), and its "pericentric" region covers approximately three-quarters of its length and consists of mostly simple satellite repeats. Its "euchromatic" portion contains single-copy genes interspersed between blocks of repetitive DNAs that in the two major autosomes are largely confined to heterochromatin (59,148). In addition to its diminutive size, or perhaps because of it, chromosome 4 has a heterochromatic quality. HP1 associates with much of chromosome 4 (149), and reporter genes carried on transposable elements inserted into chromosome 4 often show variegated expression (i.e., PEV (69,148). Furthermore, chromosome 4 does not normally undergo crossing over in female meiosis, a property it shares with pericentric heterochromatic regions.
In a number of ways, chromosome 4 shows closer affinity with the X chromosome than it does with the autosomes (see ref. 147). A recent and fascinating example of this is the putative RNA-binding protein Painting of fourth (POF), which specifically "paints" chromosome 4 (in polytene nuclei) by spreading over the chromosome in much the same way that the complex of male-specific lethal proteins and roX RNAs coats the hypertranscribed X chromosome in dosage-compensated males (150,151). In D. busckii, where the counterpart to D. melanogaster chromosome 4 is inserted at the base of the X, anti-POF antibodies paint the entire X chromosome but only in males. In D. melanogaster, POF paints the fourth chromosomes of both males and females, although inexplicably the Pof gene (on chromosome 2 at 60E) is expressed at far higher levels in males compared to females. Assuming the D. busckii constitution to be ancestral, Larsson et al. (147) supposed that D. busckii POF may function in X chromosome dosage compensation and that D. melanogaster may have adapted that function to help regulate expression of chromosome 4 genes in their heterochromatic environment.
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