The maturation of nascent RNA is closely linked to the transcription process. It is well known for animals and plants that RNA polymerase II (RNAPII) elongation rate, pausing, and termination steps may affect the quality and quantity of its final product: mature mRNA. Pre-mRNA splicing, incorporation of RNA modifications, as well as 3' end maturation, are co-transcriptional. However, plant miRNA biogenesis was considered post-transcriptional and localized in so-called D-bodies (Dicing bodies) in the cell nucleus for years. Our studies clearly show that in Arabidopsis, miRNA production occurs during transcription and is tightly regulated at multiple levels, including RNA modifications. Small RNA precursors contain modified nucleotides including m6A and pseudouridine (Ψ). Both modifications are known to be important for maintaining the proper secondary structure of RNA. Moreover, we developed assays to detect Ψ in short RNA sequences, demonstrating its presence in Arabidopsis miRNAs and their precursors. We also detect substantial enrichment in germline small RNAs - epigenetically activated siRNAs (easiRNAs) in Arabidopsis pollen. Pseudouridylated easiRNAs are localized to sperm cells, and we found that PAUSED (PSD), the plant homolog of Exportin-t, interacts genetically with Ψ and is required for the transport of easiRNAs into sperm cells from the vegetative nucleus. We further show that Exportin-t is required for the triploid block: chromosome dosage-dependent seed lethality that is epigenetically inherited from pollen. Thus, Ψ has a conserved role in marking inherited small RNAs in the germline.