Programmed DNA elimination in multicellular organisms

Abstract

Genetic information typically remains constant in all cells throughout the life cycle of most organisms. However, there are exceptions where DNA elimination is an integral, developmental program for some organisms, associated with generating distinct germline versus somatic genomes. Programmed DNA elimination occurs in unicellular ciliates and diverse metazoa ranging from nematodes to vertebrates. DNA elimination can occur through chromosome breakage and selective loss of chromosome regions or the elimination of individual chromosomes. Recent studies provide compelling evidence that DNA elimination is a novel form of gene silencing, dosage compensation, and sex determination. Further identification of the eliminated sequences, genome changes, and in depth characterization of this phenomenon in diverse metazoans is needed to shed new light on the functions and mechanisms of this regulated process.

Fig. 1. Programmed DNA elimination in multicellular organisms

Organisms known to undergo DNA elimination are illustrated on a phylogenetic tree. The tree was constructed from 18S ribosomal RNA sequences using MEGA (v5.22) [55]. Common names are used for the groups. The tree is rooted on ciliates. Photo credits: Antonio Guillen from Water Project, Spain (ciliate S. mytilus), Colin Johnstone (nematode P. univalens), Entomart (moth P. fuliginosa), wiley library (mite M. occidentalis), James Haney (copepod M. edax), Jeremiah Smith (Sea lamprey P. marinus), Kinya G. Ota and Shigeru Kuratani (hagfish E. burgeri), wikipedia.org (Spotted ratfish H. colliei and Zebra finch T. guttata), and Joseph McKenna (bandicoot I. macrourus). The year that DNA elimination was discovered in each group of organisms is noted.

Fig. 2. Chromatin diminution in Parascaris and Ascaris

A and B. P. univalens embryos. A. 1-cell embryo showing the single pair of germline chromosomes. B. 4-cell embryo with two cells (outlined in red) undergoing diminution. The retained portions of the germline chromosomes are fragmented into many smaller chromosomes (small arrows). The heterochromatic arms that will be eliminated (big arrows) remain visible. C and D. A. suum embryos. C. 4-cell embryo with two cells undergoing chromatin diminution. D. 6-cell embryo with one cell undergoing chromatin diminution. Note that DNA to be eliminated is present as fragments (artificially colored red) between chromosomes segregating in early anaphase (C); DNA fragments (red) derived from a previous cell diminution can be seen in the cytoplasm of cells to the right (D).