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Resetting of 24-nt siRNA landscape is initiated in the unicellular zygote in rice

The zygote, a totipotent stem cell, constitutes a critical stage of the life cycle for all sexually reproducing organisms. It is produced by fusion of two differentiated cells, egg and sperm, that in plants have radically different siRNA transcriptomes from each other and from multicellular embryos. Here we examined the small RNA transcriptome of unicellular rice zygotes. We find that the overall 24-nt siRNA landscape in the zygote resembles that of the unfertilized egg cell, consistent with maternal carry-over. A large fraction (∼75%) of the siRNAs in the zygote arise from a small proportion (∼2%) of siRNA loci, which corresponded to similar loci in the egg cell and ovary. However, these highly expressing loci were distinct from endosperm siren loci that were detected in later stage endosperm. miRNA abundances changed rapidly after fertilization, resulting in a miRNA profile distinct from the egg cell. Notably, the de novo 24-nt siRNAs expressed by the zygote had characteristics of canonical siRNAs, such as proximity to genes and tendency to overlap TIR DNA transposable elements, and resembled seedling siRNA loci, indicating a return to the canonical siRNA profile typical of vegetative tissues. Taken together, our results suggest that resetting of the gametic epigenome towards the canonical vegetative profile is initiated before the first embryonic division.