Functional Significance of Satellite DNAs: Insights From Drosophila

Abstract

Since their discovery more than 60 years ago, satellite repeats are still one of the most enigmatic parts of eukaryotic genomes. Being non-coding DNA, satellites were earlier considered to be non-functional "junk," but recently this concept has been extensively revised. Satellite DNA contributes to the essential processes of formation of crucial chromosome structures, heterochromatin establishment, dosage compensation, reproductive isolation, genome stability and development. Genomic abundance of satellites is under stabilizing selection owing of their role in the maintenance of vital regions of the genome - centromeres, pericentromeric regions, and telomeres. Many satellites are transcribed with the generation of long or small non-coding RNAs. Misregulation of their expression is found to lead to various defects in the maintenance of genomic architecture, chromosome segregation and gametogenesis. This review summarizes our current knowledge concerning satellite functions, the mechanisms of regulation and evolution of satellites, focusing on recent findings in Drosophila. We discuss here experimental and bioinformatics data obtained in Drosophila in recent years, suggesting relevance of our analysis to a wide range of eukaryotic organisms.

Keywords: Drosophila; centromere; chromosome segregation; heterochromatin; meiotic drive; reproductive isolation; satellites; segregation distortion.

FIGURE 1

Scheme of the putative contribution of 359-bp satellite RNAs to CENP-A and CENP-C deposition at the centromeres of Drosophila melanogaster. The stable association of CENP-C and CENP-A with the centromere ensured by the presence of satellite transcripts leads to the formation of a functional kinetochore and subsequent accurate segregation of chromosomes in mitosis.

FIGURE 2

(A) Representation of chromosomes 2 of D. melanogaster indicating relative positions of components of the SD complex. Top: distorting chromosome 2 carries Sd, Segregation Distorter; Rspⁱ, Responder i (insensitive); E(SD), Enhancer of Segregation Distorter; M(SD), Modifier of Segregation Distorter; and St(SD), Stabilizer of Segregation Distorter. Bottom: non-distorting SD⁺ chromosome 2 contains wild-type loci Sd⁺, E(Sd)⁺, M(SD)⁺, and St(SD)⁺ and Rsp^s (sensitive) allele. (B) Top: Overview of SD action during Drosophila spermatogenesis. At the apical testis tip (leftward) germline stem cells (red) are located adjacent to the hub (green) and are surrounded by two somatic cyst cells (gray). One of the daughter cells of the germline stem cell, the spermatogonium, undergoes four mitotic divisions to finally create a cyst of 16 spermatocytes. Mature spermatocytes synchronously enter meiosis producing 64 haploid round spermatids. The spermatids nuclei undergo strong condensation, owing to exchanging histones for protamines. The nuclei bearing the Rsp^s allele (orange) fail to properly condense during the individualization process and are discarded in the waste bag, whereas Sd-bearing spermatids (blue) become mature sperm and enter the seminal vesicle, where they are stored until copulation. Bottom: expression patterns of PIWI subfamily proteins, Piwi, Aubergine, and AGO3, in premeiotic germline cells of the testes.

FIGURE 3

Crosses between D. simulans females and D. melanogaster males produce viable F1 male hybrids, whereas F1 hybrid females die as embryos. The X-linked Zhr locus containing a tremendous 359-bp satellite block causes hybrid lethality by inducing chromosomal segregation defects in early embryos owing the failure of the 359-bp satellites to maintain proper heterochromatin structure. Sex chromosomes inherited from D. melanogaster are shown in gray, from D. simulans – in light green. D. melanogaster Zhr locus marked by red, as well as a small block of the 360-bp repeat variant in the pericentromeric region of D. simulans X chromosome.

FIGURE 4

The main functions of satellites in the Drosophila genome.