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Initiating and interfering with silencing of transposons

Final Report Summary - I2ST (Initiating and interfering with silencing of transposons)

Higher eukaryotic genomes, particularly plant genomes, are littered with transposons and their derived fragments. Although highly abundant, the vast majority of these mobile genetic elements are not expressed as host genomes have evolved silencing mechanisms to neutralize the inherent mutagenic potential of transposon activity. The I2ST project aimed at bringing new insights into how transposons have been so successful in colonizing host genomes, how they are kept under tight control and can be unleashed thereby contributing to genome plasticity and environmental adaptation.
We have reproduced the invasion of an Arabidopsis naïve genome by a new retrotransposon. We found that the new transposon increases its copy number until it reaches ~40-60 copies. Transcription of the transposon is then turned off as a consequence of small RNA-mediated DNA methylation. DNA methylation is an epigenetic mark commonly associated with silencing. Similar to variation in DNA sequence, variation in DNA methylation occurs in the wild and can impact gene and transposon expression. How distinct methylation states of genes and transposons, called epialleles, emerge, is not well understood. We found that combining identical genomes with different DNA methylation patterns in the same individual results in an epigenomic shock that is characterized by widespread changes in DNA methylation and gene expression. Many novel epialleles not found in the parents are formed at genes, while transposons often experience decreased DNA methylation associated transcriptional activation. Our work provides a scenario for the rapid and broad-scale emergence of epigenetic variation and may have implications to transposon dynamics within populations.
Screening a mutant population for silencing defective mutants, we revealed a new role for the MAIN and MAIL1 genes in maintaining transposon silencing. The MAIN and MAIL1 proteins act in complex and enforce silencing independently of DNA methylation. We found that these two factors define a previously unknown silencing pathway. These two proteins contain transposase-derived domains suggesting that transposon-derived genes have been co-opted during plant evolution to control transposon silencing. We also isolated a strong mutant of the polymerase epsilon in which silencing of heterochromatic transposons is drastically alleviated. Our work reveals that the DNA polymerase epsilon plays a crucial role in maintaining both structure and function of heterochromatin.
There were some examples indicating that transposons’ expression is under environmental influence. We found that a heat stress could induce transitory and widespread transcriptional activation of transposons independently of changes in repressive epigenetic marks, and we identified several genes required for this process.
Together, these results provide new insight into transposon silencing dynamics and open new avenues for future research in this field.