Origin of $\alpha$-satellite repeat arrays from mitochondrial molecular fossils -- sequential insertion, expansion, and evolution in the nuclear genome

TL;DR

This study uncovers that alpha satellite DNA in the nuclear genome of jewel wasp originated from mitochondrial insertions, followed by expansion and rapid evolution driven by GC-biased gene conversion, revealing a novel origin of satellite DNA.

Contribution

It provides the first evidence that nuclear satellite sequences can originate from mitochondrial DNA insertions, detailing their evolution and expansion in insects.

Findings

SatL arrays originated from mitochondrial insertions within 500,000 years

Rapid sequence evolution driven by GC-biased gene conversion

Substantial copy number expansion of satellite repeats in the nuclear genome

Abstract

Alpha satellite DNA is large tandem arrays of 150-400 bp units, and its origin remains an evolutionary mystery. In this research, we identified 1,545 alpha-satellite-like (SatL) repeat units in the nuclear genome of jewel wasp Nasonia vitripennis. Among them, thirty-nine copies of SatL were organized in two palindromic arrays in mitochondria, resulting in a 50% increase in the genome size. Strikingly, genomic neighborhood analyses of 1,516 nuclear SatL repeats revealed that they are located in NuMT (nuclear mitochondrial DNA) regions, and SatL phylogeny matched perfectly with mitochondrial genes and NuMT pseudogenes. These results support that SatL arrays originated from ten independent mitochondria insertion events into the nuclear genome within the last 500,000 years, after divergence from its sister species N. giraulti. Dramatic repeat GC-percent elevation (from 33.9% to 50.4%) is a hallmark of rapid SatL sequence evolution in mitochondria due to GC-biased gene conversion facilitated by the palindromic sequence pairing of the two mitochondrial SatL arrays. The nuclear SatL repeat arrays underwent substantial copy number expansion, from 12-15 (SatL1) to over 400 copies (SatL4). The oldest SatL4B array consists of four types of repeat units derived from deletions in the AT-rich region of ancestral repeats, and complex high-order structures have evolved through duplications. We also discovered similar repeat insertions into the nuclear genome of Muscidifurax, suggesting this mechanism can be common in insects. This is the first report of the mitochondrial origin of nuclear satellite sequences, and our findings shed new light on the origin and evolution of satellite DNA.