Waste not, want not: Does DNA elimination fuel gene amplification during development in ciliates?

The sexual phase of the life cycle in ciliates represents a developmental program with several parallels to multicellular development. During this pathway an undifferentiated zygotic nucleus gives rise to two lineages, a germinal micronuclear lineage and a somatic macronuclear lineage. The development of nascent macronuclei (or ‘anlagen’) from micronuclei involves a highly regulated set of DNA rearrangements which include chromosomal breakage, telomere addition, DNA elimination and gene amplification. Here we review recent progress in identifying stage-specific polypeptides from Tetrahymena analgen that are likely to be involved in these rearrangements. One of the more abundant of these polypeptides, p65, participates in the formation of DNA-containing structures that resemble developing nucleoli. We propose a simple model in which the micronuclear gene segments that are not to be included in the mature macronuclear genome are first digested in these p65-based particles, and then the resulting nucleotides are ‘recycled’ by using them to amplify rDNA. Our ‘intranuclear recycling’ model suggests a possible compartmentalization strategy that functions to ensure adequate rDNA/rRNA production during macronuclear development. Implications of the model for programmed DNA rearrangements and nucleolar biogenesis are discussed.