The piggyBac transposon-derived genes TPB1 and TPB6 mediate essential transposon-like excision during the developmental rearrangement of key genes in Tetrahymena thermophila

Genes Dev. 2016 Dec 15;30(24):2724-2736. doi: 10.1101/gad.290460.116.


Ciliated protozoans perform extreme forms of programmed somatic DNA rearrangement during development. The model ciliate Tetrahymena thermophila removes 34% of its germline micronuclear genome from somatic macronuclei by excising thousands of internal eliminated sequences (IESs), a process that shares features with transposon excision. Indeed, piggyBac transposon-derived genes are necessary for genome-wide IES excision in both Tetrahymena (TPB2 [Tetrahymena piggyBac-like 2] and LIA5) and Paramecium tetraurelia (PiggyMac). T. thermophila has at least three other piggyBac-derived genes: TPB1, TPB6, and TPB7 Here, we show that TPB1 and TPB6 excise a small, distinct set of 12 unusual IESs that disrupt exons. TPB1-deficient cells complete mating, but their progeny exhibit slow growth, giant vacuoles, and osmotic shock sensitivity due to retention of an IES in the vacuolar gene DOP1 (Dopey domain-containing protein). Unlike most IESs, TPB1-dependent IESs have piggyBac-like terminal inverted motifs that are necessary for excision. Transposon-like excision mediated by TPB1 and TPB6 provides direct evidence for a transposon origin of not only IES excision machinery but also IESs themselves. Our study highlights a division of labor among ciliate piggyBac-derived genes, which carry out mutually exclusive categories of excision events mediated by either transposon-like features or RNA-directed heterochromatin.

Keywords: Tetrahymena; domesticated transposon; piggyBac; programmed genome rearrangement; vacuoles.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, N.I.H., Extramural

MeSH terms

  • DNA Transposable Elements / genetics*
  • Gene Expression Regulation, Developmental
  • Gene Knockout Techniques
  • Gene Rearrangement / genetics*
  • Genes, Protozoan / genetics*
  • Genome, Protozoan / genetics*
  • Life Cycle Stages
  • Protozoan Proteins / genetics
  • Protozoan Proteins / metabolism*
  • Tetrahymena thermophila / genetics*
  • Tetrahymena thermophila / growth & development
  • Vacuoles / genetics


  • DNA Transposable Elements
  • Protozoan Proteins