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 arise from the products of meiosis by mitotic division, and a number of companion cells also differentiate resembling 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. In ovules, mutants in this same small RNA pathway result in differentiation of additional ameiotic diploid germ cells, as well as TE activation in the egg. Aberrant germ cell specification has profound implications for plant reproduction, including the production of clonal unreduced seeds (apomixis). We will investigate the mechanism of germline reprogramming in plants, and the function of small RNA in specification of germ cell identity. We will also investigate the transgenerational inheritance of epialleles when reprogramming goes awry. We have preliminary evidence that systemically mobile small RNA accumulate in the gametes, from which they are passed into the fertilized zygote, providing a mechanism for transgenerational inheritance.
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 Methylation1 which, 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. We will determine whether these small RNA are responsible for sporadic gene methylation and epigenetic inheritance. We will also investigate their role in meiosis and germ cell fate.
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