Arabidopsis proteins with a transposon-related domain act in gene silencing

Abstract

Transposable elements (TEs) are prevalent in most eukaryotes, and host genomes have devised silencing strategies to rein in TE activity. One of these, transcriptional silencing, is generally associated with DNA methylation and short interfering RNAs. Here we show that the Arabidopsis genes MAIL1 and MAIN define an alternative silencing pathway independent of DNA methylation and short interfering RNAs. Mutants for MAIL1 or MAIN exhibit release of silencing and appear to show impaired condensation of pericentromeric heterochromatin. Phylogenetic analysis suggests not only that MAIL1 and MAIN encode a retrotransposon-related plant mobile domain, but also that host plant mobile domains were captured by DNA transposons during plant evolution. Our results reveal a role for Arabidopsis proteins with a transposon-related domain in gene silencing.

Transposable Element Domestication As an Adaptation to Evolutionary Conflicts

“…In Arabidopsis , two genes MAIL1 and MAIN encode related proteins that appear to be evolutionarily derived from a subset of Ty3/ gypsy retrotransposons found in angiosperms [48]. These proteins might have been initially captured from the host by these elements, but appear to have been reclaimed to partake in an epigenetic silencing pathway that transcriptionally represses a broad array of TEs [48].…”

“…These proteins might have been initially captured from the host by these elements, but appear to have been reclaimed to partake in an epigenetic silencing pathway that transcriptionally represses a broad array of TEs [48]. Genetic loss of these genes resulted in impaired condensation of pericentromeric heterochromatin and upregulation of TE transcription suggesting their protein products are acting as transcriptional repressors.…”

“…The molecular mechanisms by which MAIL1 and MAIN promote the formation of silent chromatin remain to be characterized, but involve a molecular pathway independent of small-interfering RNAs (see Glossary) and DNA methylation. It is intriguing that proteins related to MAIL1 and MAIN seem to have been acquired by TEs multiple times, including DNA transposons of the Mutator -like superfamily, which may reflect a counter-defense strategy deployed by these elements [48]. …”

The plant mobile domain proteins MAIN and MAIL1 interact with the phosphatase PP7L to regulate gene expression and silence transposable elements in Arabidopsis thaliana

“…The main-2 and mail1-1 null mutants show similar developmental phenotypes, and transcriptomic analyses have revealed that many TEs, including ATCOPIA28 , are overexpressed in these two mutants (S2A and B Fig, and S2 Table) [17]. In addition, several genes are misregulated in the two pmd mutants (S2C and D Fig, and S2 Table).…”

“…More recently, the A. thaliana plant mobile domain (PMD) proteins MAINTENANCE OF MERISTEM (MAIN) and MAIN-LIKE 1 (MAIL1) were identified as new factors required for TE silencing [17]. In addition, these two proteins have been involved in genome stability, and regulation of developmental processes such as cell division and differentiation [18, 19].…”