Programmed DNA Elimination in Vertebrates

Abstract

Over the last few decades, an increasing number of vertebrate taxa have been identified that undergo programmed genome rearrangement, or programmed DNA loss, during development. In these organisms, the genome of germ cells is often reproducibly different from the genome of all other cells within the body. Although we clearly have not identified all vertebrate taxa that undergo programmed genome loss, the list of species known to undergo loss now represents ∼10% of vertebrate species, including several basally diverging lineages. Recent studies have shed new light on the targets and mechanisms of DNA loss and their association with canonical modes of DNA silencing. Ultimately, expansion of these studies into a larger collection of taxa will aid in reconstructing patterns of shared/independent ancestry of programmed DNA loss in the vertebrate lineage, as well as more recent evolutionary events that have shaped the structure and content of eliminated DNA.

Keywords: evolution; genome; programmed DNA loss; programmed genome rearrangement; vertebrate.

Figure 1

Integration of programmed DNA elimination with development. Germline-specific chromosomes/segments are shown in red. Functions encoded on these genes are limited to the germline and irreversibly silenced in somatic cells.

Figure 2

A phylogeny of the vertebrates, highlighting taxa known to undergo programmed DNA elimination (red); unknown taxa/lineages appear in black or gray. Divergence dates are taken from References , , and .

Figure 3

Differences between lamprey germline and somatic karyotypes. (a) A meiotic metaphase I chromosome spread. (b) A mitotic metaphase spread generated from a 16-day-old embryo. Chromosomes were stained with DAPI and labeled with fluorescence in situ hybridization probes to the Germ1 repeat (green) and a laser capture (LC; red) probe, generated from eliminated chromatin (41, 120). Both Germ1 and LC probes hybridize with multiple tetrads in meiotic metaphase I, whereas signals are observed on only one pair of mitotic chromosomes (indicated with arrows). Hybridization of the LC probe to somatic cells yields weaker signals that are only slightly brighter than background fluorescence, in contrast to hybridization patterns on meiotic chromosomes.

Figure 4

Chromosome elimination during sea lamprey development. Embryos have an initial haploid chromosome number of N = 96. Chromosome elimination is initiated after the sixth cleavage division at one day postfertilization (dpf). Presomatic cells isolate 12 whole chromosomes that are packaged into micronuclei, which initially accumulate silencing marks on histones and then 5-methylcytosine. Primary nuclei show signs of epigenetic silencing later in development, at the time that eliminated chromosomes are being degraded within micronuclei.

Figure 5

Schematic overview of epigenetic modifications that are visible on the germline-restricted chromosome during male meiosis of the zebra finch and Bengalese finch (6, 11, 63). Differing results from Schoenmakers et al. (63) (*) and Goday & Pigozzi (11) (⌖).