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

Abstract

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.

The Evolutionary Volte-Face of Transposable Elements: From Harmful Jumping Genes to Major Drivers of Genetic Innovation

“…Later, it was shown that MAIN and MAIL1 were required for the proper expression of a common subset of genes, as well as TE silencing [ 104 ] ( Figure 1 D). MAIN and MAIL1 physically interact together, as well as with a putative serine/threonine phosphoprotein phosphatase (PPP) called PP7-LIKE (PP7L), and the three mutants show similar developmental and molecular phenotypes, including TE silencing defects [ 107 , 108 ]. Genome-wide level of 5mC is mostly unchanged in main and mail1 mutants, with the notable exception of a slight increase in CHG methylation at pericentromeric regions and in chromosome arm TEs [ 108 ].…”

“…MAIN and MAIL1 physically interact together, as well as with a putative serine/threonine phosphoprotein phosphatase (PPP) called PP7-LIKE (PP7L), and the three mutants show similar developmental and molecular phenotypes, including TE silencing defects [ 107 , 108 ]. Genome-wide level of 5mC is mostly unchanged in main and mail1 mutants, with the notable exception of a slight increase in CHG methylation at pericentromeric regions and in chromosome arm TEs [ 108 ]. Importantly, this modest non-CG hypermethylation does not correlate with changes in TE expression observed in the mutant [ 108 ].…”

“…Genome-wide level of 5mC is mostly unchanged in main and mail1 mutants, with the notable exception of a slight increase in CHG methylation at pericentromeric regions and in chromosome arm TEs [ 108 ]. Importantly, this modest non-CG hypermethylation does not correlate with changes in TE expression observed in the mutant [ 108 ]. Synergistic effects were described between MAIN and 5mC pathways.…”

“…Synergistic effects were described between MAIN and 5mC pathways. The main drm1 drm2 cmt3 quadruple mutant showed exacerbation of TE silencing defects, with a number being specifically derepressed in this mutant background [ 108 ]. Altogether, these results suggest that together with MAIL1 and PP7L, MAIN would define a distinct epigenetic pathway that cooperates with DRM2- and CMT3-mediated 5mC to silence TEs.…”

“…Another strategy was described for the class II VANDAL21 TE that encodes the silencing suppressor VANC21, specifically promoting DNA hypomethylation at VANDAL21 TE sequences [ 133 , 134 ]. Finally, the PMD MAIN and MAIL1 TE silencing effectors are phylogenetically related to TE-encoded proteins, suggesting that TEs may produce their own PMD proteins as a counter-silencing strategy [ 104 , 108 ]. Altogether, these studies illustrate the evolutionary arms race between TEs and their host, relying on a fine balance between TE fitness and host genome integrity.…”