Transposable elements (TEs) are DNA repeats that must remain silenced to ensure cell integrity. Several epigenetic pathways including DNA methylation and histone modifications are involved in the silencing of TEs, and in the regulation of gene expression. In Arabidopsis thaliana, the TE-derived plant mobile domain (PMD) proteins have been involved in TE silencing, genome stability, and control of developmental processes. Using a forward genetic screen, we found that the PMD protein MAINTENANCE OF MERISTEMS (MAIN) acts synergistically and redundantly with DNA methylation to silence TEs. We found that MAIN and its close homolog MAIN-LIKE 1 (MAIL1) interact together, as well as with the phosphoprotein phosphatase (PPP) PP7-like (PP7L). Remarkably, main, mail1, pp7l single and mail1 pp7l double mutants display similar developmental phenotypes, and share common subsets of upregulated TEs and misregulated genes. Finally, phylogenetic analyses of PMD and PP7-type PPP domains among the Eudicot lineage suggest neo-association processes between the two protein domains to potentially generate new protein function. We propose that, through this interaction, the PMD and PPP domains may constitute a functional protein module required for the proper expression of a common set of genes, and for silencing of TEs.

Transposable elements (TEs) are self-replicating DNA elements that constitute major fractions of eukaryote genomes. Their ability to transpose can modify the genome structure with potentially deleterious effects. To repress TE activity, host cells have developed numerous strategies, including epigenetic pathways, such as DNA methylation or histone modifications. Although TE neo-insertions are mostly deleterious or neutral, they can become advantageous for the host under specific circumstances. The phenomenon leading to the appropriation of TE-derived sequences by the host is known as TE exaptation or co-option. TE exaptation can be of different natures, through the production of coding or non-coding DNA sequences with ultimately an adaptive benefit for the host. In this review, we first give new insights into the silencing pathways controlling TE activity. We then discuss a model to explain how, under specific environmental conditions, TEs are unleashed, leading to a TE burst and neo-insertions, with potential benefits for the host. Finally, we review our current knowledge of coding and non-coding TE exaptation by providing several examples in various organisms and describing a method to identify TE co-option events.

ABSTRACTTransposable elements (TEs) are DNA repeats that must remain silenced to ensure cell integrity. Several epigenetic pathways including DNA methylation and histone modifications are involved in the silencing of TEs, and in the regulation of gene expression. In Arabidopsis thaliana, the TE-derived plant mobile domain (PMD) proteins have been involved in TE silencing, genome stability, and control of developmental processes. Using a forward genetic screen, we found that the PMD protein MAINTENANCE OF MERISTEMS (MAIN) acts synergistically and redundantly with DNA methylation to silence TEs. We found that MAIN and its close homolog MAIN-LIKE 1 (MAIL1) interact together, as well as with the phosphoprotein phosphatase (PPP) PP7-like (PP7L). Remarkably, main, mail1, pp7l single and mail1 pp7l double mutants display similar developmental phenotypes, and share common subsets of upregulated TEs and misregulated genes. Finally, phylogenetic analyses of PMD and PP7-type PPP domains among the Eudicot lineage suggest neo-association processes between the two protein domains to potentially generate new protein function. We propose that, through this interaction, the PMD and PPP domains may constitute a functional protein module required for the proper expression of a common set of genes, and for silencing of TEs.AUTHOR SUMMARYThe plant mobile domain (PMD) is a protein domain of unknown function that is widely spread in the angiosperm plants. Although most PMDs are associated with repeated DNA sequences called transposable elements (TEs), plants have domesticated the PMD to produce genic versions that play important roles within the cell. In Arabidopsis thaliana, MAINTENANCE OF MERISTEMS (MAIN) and MAIN-LIKE 1 (MAIL1) are genic PMDs that are involved in genome stability, developmental processes, and silencing of TEs. The mechanisms involving MAIN and MAIL1 in these cellular processes remain elusive. Here, we show that MAIN, MAIL1 and the phosphoprotein phosphatase (PPP) named PP7-like (PP7L) interact to form a protein complex that is required for the proper expression of genes, and the silencing of TEs. Phylogenetic analyses revealed that PMD and PP7-type PPP domains are evolutionary connected, and several plant species express proteins carrying both PMD and PPP domains. We propose that interaction of PMD and PPP domains would create a functional protein module involved in mechanisms regulating gene expression and repressing TEs.

Silencing of transposable elements (TEs) is an essential process to maintain genomic integrity within the cell. InArabidopsis, together with canonical epigenetic pathways such as DNA methylation and modifications of histone tails, the plant mobile domain (PMD) proteins MAINTENANCE OF MERISTEMS (MAIN) and MAIN-LIKE 1 (MAIL1) are involved in TE silencing. In addition, the MICRORCHIDIA (MORC) ATPases, including MORC1, are important cellular factors repressing TEs. Here, we describe the genetic interaction and connection between the PMD and MORC pathways by showing thatMORC1expression is impaired inmainandmail1mutants. Transcriptomic analyses of higher order mutant plants combiningpmdandmorc1mutations, andpmdmutants in whichMORC1expression is restored, show that the silencing defects of a subset of TEs inpmdmutants are most likely the consequence ofMORC1down-regulation. Besides, a significant fraction of up-regulated TEs inpmdmutants are not targeted by the MORC1 pathway.