Public Service by a Selfish Gene: A Domesticated Transposase Antagonizes Polycomb Function

Eukaryotic genomes are littered with transposable elements (TEs)—“selfish” genetic entities capable of increasing copy numbers through transposition to account for large fractions of the nuclear DNA. To minimize the mutagenic effects of transposition, host organisms have evolved various mechanisms to repress TE-encoded genes (TEGs) both transcriptionally through chromatin modifications and post-transcriptionally through RNA interference. Over time, silenced TEs accumulate genetic mutations, become immobilized, and are eliminated from the genome by recombination or decay into intergenic DNA. But can immobilized TEGs fortuitously acquire cellular functions that are beneficial to the host and become a useful fixture of the genome? In a recent issue of PLOS Genetics, Turck, Goodrich, and colleagues describe a clear example of this process, in which a transposase-derived gene functions to antagonize transcriptional repression by the Polycomb group (PcG) genes in Arabidopsis thaliana [1]. PcG genes play critically important roles in regulating plant development by targeting thousands of genes for transcriptional repression through trimethylation of lysine 27 on histone H3 (H3K27me3) [2]. In Arabidopsis, PcG function requires two classes of protein complexes: Polycomb Repressive Complexes 1 and 2 (PRC1 and PRC2, respectively). The enzymatic complex PRC2 contains one of the three H3K27 trimethyltransferases, MEDEA (MEA), CURLY LEAF (CLF), and SWINGER (SWN), whereas the PRC1 complex includes the H3K27me3-binding protein LIKE HETEROCHROMATIN PROTEIN 1 (LHP1). To better understand the mechanisms that may counteract PcG repression, two independent suppressor screens were performed to identify mutants that could revert the developmental and transcriptional defects of the CLF and LHP1 mutants, respectively [1,3]. One gene named ANTAGONIST OF LIKE HETEROCHROMATIN PROTEIN 1 (ALP1) was isolated from both screens, indicating that it likely functions broadly in antagonizing PcG repression [1,3]. This notion is supported by several lines of evidence: (1) alp1 suppresses the developmental phenotypes of clf; (2) a significant faction of genes overexpressed in clf are no longer overexpressed in alp1 clf; (3) ALP1 functions upstream of PcG-repressed genes (e.g., AGAMOUS); (4) many PcG-target genes are down-regulated in alp1 when normal PcG activity is present; (5) alp1 enhances the defects of several mutants of trithorax group (trxG) genes involved in counteracting PcG repression; and (6) ALP1 physically interacts with PRC2 in planta. Taken together, these results strongly indicate that ALP1 is generally required to antagonize PcG repression at a large number of developmentally important genes [1]. Interestingly, ALP1 encodes a protein that is highly similar to the transposases (TPases) of the PIF/Harbinger superfamily of DNA TEs [1,3]. The first active member of the superfamily, P Instability Factor (PIF), was identified in maize as repeated mutagenic insertions into the