Cold Spring Harbor Laboratory, NY, USA
After completing his undergraduate and graduate studies in England and a postdoctoral period at UC Berkeley, Rob Martienssen is currently a Howard Hughes Medical Institute–Gordon and Betty Moore Foundation investigator as well as a professor at Cold Spring Harbor Laboratory. He is a pioneer in the study of epigenetics and investigates mechanisms involved in gene regulation and stem cell fate in yeast and model plants including Arabidopsis and maize. He and his colleagues have shed light on a phenomenon called position-effect variegation, caused by inactivation of a gene positioned near densely packed chromosomal material called heterochromatin. They have discovered that small RNA molecules arising from repeating genetic sequences program heterochromatin formation. Martienssen and colleagues have described a remarkable process by which “companion cells” to sperm in plant pollen grains provide them with instructions that protect sperm DNA from transposon damage. They found that some of these epigenetic marks could be inherited in the next generation.
Epigenetic inheritance is more widespread in plants than in mammals, in part because mammals erase epigenetic information each generation by germline reprogramming. To assess the extent of germline reprogramming in plants, we sequenced the methylome from sperm cells (SC), the vegetative nucleus (VN), and the precursor microspore from developing haploid pollen. We found that asymmetric CHH methylation is lost in microspores and sperm cells, but restored in the VN and in fertilized seed. In the VN symmetric CG methylation is lost from targets of the DNA glycosylases DEMETER (DME) and REPRESSOR OF SILENCING 1 (ROS1) including transposons near imprinted genes, which contributes to imprinting via RNA directed DNA methylation and 24nt siRNA. In contrast, most active transposons give rise to 21nt “epigenetically activated” small RNA in DECREASE IN DNA METHYLATION 1 (DDM1) mutants, in tissue culture and in the VN, which loses heterochromatin. Biogenesis of 21nt epigenetically activated siRNA requires miRNA and RNA DEPENDENT RNA POLYMERASE 6. Loss of heterochromatin in the VN is not the direct result of loss of DNA methylation but instead may be due to histone replacement with variants resistant to modiﬁcation. Thus genome reprogramming in pollen contributes to epigenetic inheritance, transposon silencing, and imprinting, guided by small RNA.
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