The germlines of plants and animals undergo genome reprogramming in order to reset epigenetic marks that would otherwise interfere with pluripotency of the zygote. Perhaps chief among these marks are epigenetic modifications of transposable elements (TE), which make up a majority of most eukaryotic genomes. We have found that small interfering RNA derived from heterochromatin plays a key role in germline reprogramming in plants, and there is mounting evidence for a similar phenomenon in animals. Germ cells in plants differentiate from the products of meiosis by mitotic division, along with companion cells that resemble nurse cells and other support cells in animals. We have found that reprogramming of the pollen grain companion cell nucleus (the vegetative nucleus or VN) results in transposon activation, and that a new class of epigenetically activated small interfering RNA (easiRNA) accumulate in sperm cells, that have the potential to silence these same transposons. We have recently found that genome reprogramming depends on DNA methylation, but also on the deposition and modification of specific histone variants, that is likey the result of cell cycle dependent chromatin remodeling. Epigenetic inheritance is far more widespread in plants than in mammals, although the mechanisms are largely conserved, so that plants provide an excellent system to study their origin. We will investigate the mechanism of germline reprogramming in plants, and the transgenerational consequences when reprogramming goes awry.
There is a growing body of evidence that environmental factors can have transgenerational effects on human health. However, the mechanism of epigenetic transmission and its impact on gene expression in the next generation is still unknown. Genome reprogramming is fundamental to normal development of the germline and early embryo. Both primordial germ cells and embryos lose DNA methylation from transposons, and gain methylation of imprinted genes. Similar reprogramming of the cancer genome can lead to silencing of tumor suppressor genes. Focusing on plants, we have found mobile small RNA signals from transposons that arise following reprogramming in the germline. These small RNA depend on the chromatin remodeler Decrease in DNA Methylation1which, like its homologs in mouse and humans, is expressed in sperm cells, and a similar interaction between small RNA, transposon silencing and genome reprogramming has recently emerged in the mammalian germline. By manipulating key reprogramming mechanisms, such as DNA methylation and chromatin remodelling, we will determine how these small RNA contribute to epigenetic inheritance.
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