Delete and survive: strategies of programmed genetic material elimination in eukaryotes

Abstract

Genome stability is a crucial feature of eukaryotic organisms because its alteration drastically affects the normal development and survival of cells and the organism as a whole. Nevertheless, some organisms can selectively eliminate part of their genomes from certain cell types during specific stages of ontogenesis. This review aims to describe the phenomenon of programmed DNA elimination, which includes chromatin diminution (together with programmed genome rearrangement or DNA rearrangements), B and sex chromosome elimination, paternal genome elimination, parasitically induced genome elimination, and genome elimination in animal and plant hybrids. During programmed DNA elimination, individual chromosomal fragments, whole chromosomes, and even entire parental genomes can be selectively removed. Programmed DNA elimination occurs independently in different organisms, ranging from ciliate protozoa to mammals. Depending on the sequences destined for exclusion, programmed DNA elimination may serve as a radical mechanism of dosage compensation and inactivation of unnecessary or dangerous genetic entities. In hybrids, genome elimination results from competition between parental genomes. Despite the different consequences of DNA elimination, all genetic material destined for elimination must be first recognised, epigenetically marked, separated, and then removed and degraded.

Keywords: B chromosomes; asexual hybrids; chromatin diminution; chromosomal lagging; micronuclei; programmed DNA elimination; sex chromosomes.

Fig 1

Overview of programmed DNA elimination during ontogenesis in multicellular model organisms. Normal ontogenesis without programmed DNA elimination is represented in the centre. Chromatin diminution, elimination of supernumerary and sex chromosomes, paternal genome elimination, parasitically induced genome elimination, and elimination of one parental genome in hybrids are shown according to the timing of elimination during ontogenesis. For specific details of each of the cases of programmed DNA elimination see Figs 2, 3, 4, 5, 6, 7, 8. GRC, germline‐restricted chromosome; PSR, paternal sex ratio.

Fig 2

Chromatin diminution in sea lamprey (A) and parasitic nematode (B). See Fig. 1 for key. The image of the four‐cell embryo indicates that elimination takes place during early developmental stages. Eliminated (red) and retained (violet) chromosomes and their fragments are shown in the karyotype and during mitosis in the boxed images on the right. (A) In sea lamprey, the eliminated fragments or whole chromosomes do not attach to the spindle and lag during anaphase. Progenitors of germ cells keep their genome intact. (B) During chromatin diminution in progenitors of somatic cells in nematodes, the eliminated fragments of holocentric chromosomes do not attach to the spindle and are eliminated during anaphase. Progenitors of germ cells keep their genome intact. See text for further details.

Fig 3

Supernumerary chromosome elimination in goatgrass (A), sciarid flies (B, C) and the zebra finch (D, E). Eliminated (red) and retained (violet) chromosomes are indicated in karyotypes in cells during interphase, in mitosis, and in meiosis in the boxed images on the right. The images of the four‐cell embryo or gonad indicate that elimination takes place during early developmental stages or during gametogenesis, respectively. (A) Elimination of the B chromosome occurs in proto‐root cells of the plant embryo but not in cells from the upper part of the plant. (B, D) Elimination of the B chromosome occurs only in progenitors of somatic cells of the embryo in sciarid flies and the zebra finch. (C) Elimination of the B chromosome via budding from the interphase nucleus occurs in germ cells of sciarid flies. (E) Elimination of the B chromosome during meiosis in zebra finch males. See text for further details.

Fig 4

Sex chromosome elimination in bandicoots (A) and sciarid flies (A, B). Eliminated (red) and retained (violet) chromosomes are indicated in karyotypes in cells during interphase and in mitosis in the boxed images on the right. The images of the four‐cell embryo or gonad indicate that elimination takes place during early developmental stages or during gametogenesis, respectively. (A) Elimination of sex chromosomes only from progenitors of somatic cells occurs in the embryo in bandicoots and sciarid flies. (B) Elimination of sex chromosome via budding from the interphase nucleus in germ cells of sciarid flies. See text for further details.

Fig 5

Paternal genome elimination in mealybugs (A, B) and sciarid flies (C). Eliminated (red) and retained (violet) chromosomes are indicated in karyotypes in cells during interphase and in mitosis in the boxed images on the right. The images of the four‐cell embryo or gonad indicates that elimination takes place during early developmental stages or during gametogenesis, respectively. (A) Elimination of all chromosomes from the paternal genome in all cells of the embryo during haplodiploid sex differentiation in mealybugs. (B) Elimination of all chromosomes from the paternal genome during germ cell development in mealybugs. (C) Elimination of all chromosomes from the paternal genome during monopolar spindle formation during meiosis in sciarid flies. See text for further details.

Fig 6

Paternal genome elimination caused by the paternal sex ratio (PSR) chromosome (A) and Wolbachia infection (B). Eliminated (red) and retained (violet) chromosomes are indicated in karyotypes in mitosis in boxed images on the right. The egg and sperm images indicate that elimination takes place after fertilisation. (A) Elimination of whole paternal genome after fertilisation during PSR chromosome infection in parasitoid wasp. The PSR chromosome is indicated in blue in the sperm chromatin and in the karyotypes. The PSR chromosome escapes the elimination of all other paternal chromosomes and segregates with the maternal chromosomes. (B) Elimination of whole paternal genome after fertilisation during Wolbachia infection (blue) in a fruit fly and a parasitoid wasp. The paternal pronucleus is unable to fuse with the maternal pronucleus; paternal chromatin remains condensed during the first zygotic division. See text for further details.

Fig 7

Elimination of one of the parental genomes in interspecific plant hybrids. Eliminated (red) and retained (violet) chromosomes are indicated in the karyotype in cells during interphase and mitosis in the boxed images on the right. Elimination of whole chromosomes from the genome of one parental species during early embryonic development in plant hybrids. Chromosomal elimination due to lagging during mitosis (upper row) and budding from the interphase nucleus (lower row). See text for further details.

Fig 8

Elimination of one of the parental genomes in animal hybrids reproducing clonally via kleptogenesis (A), gynogenesis (B), androgenesis (C), hybridogenesis (D, E), and meiotic (triploid) hybridogenesis (F). Eliminated (red) and retained (violet) chromosomes are indicated in karyotypes and meiosis. The egg and sperm images indicate that elimination takes place after fertilisation; the gonad image indicates that elimination takes place during gametogenesis. (A) Elimination of the paternal (upper panel) or maternal (middle panel) genomes, or partial replacement of maternal chromosomes (lower panel) during kleptogenetic reproduction in hybrid salamanders from the genus Ambystoma. (B) Elimination of the paternal pronucleus after fusion with the maternal pronucleus (upper panel) and without fusion (lower panel) during gynogenetic reproduction in hybrid fishes from the genus Carassius. (C) Elimination of the maternal genome after fertilisation via the formation of two secondary polar bodies during androgenetic reproduction in hybrid molluscs from the genus Corbicula. (D, E) Mechanisms of parental genome elimination in hybrid water frogs from the genus Pelophylax (D) and poecilid fishes (E). (D) Chromosomes of one of the parental genomes are gradually lost via lagging during mitosis (upper row) or budding from the interphase nucleus (lower row). (E) Chromosomes of one of the parental species attach to the spindle while those of the other parental species are not capable of doing so. (F) Genome elimination during meiosis in triploid hybrid loach from the genus Misgurnus. Chromosomes from the double‐copy genome form bivalents that are able to attach to the spindle while those from the single‐copy genome form univalents that are unable to attach to the spindle, and hence are eliminated during anaphase. See text for further details.