title: miRNAs trigger widespread epigenetically activated siRNAs from transposons in Arabidopsis.
abstract: In plants, post-transcriptional gene silencing (PTGS) is mediated by DICER-LIKE 1 (DCL1)-dependent microRNAs (miRNAs), which also trigger 21-nucleotide secondary short interfering RNAs (siRNAs) via RNA-DEPENDENT RNA POLYMERASE 6 (RDR6), DCL4 and ARGONAUTE 1 (AGO1), whereas transcriptional gene silencing (TGS) of transposons is mediated by 24-nucleotide heterochromatic (het)siRNAs, RDR2, DCL3 and AGO4 (ref. 4). Transposons can also give rise to abundant 21-nucleotide 'epigenetically activated' small interfering RNAs (easiRNAs) in DECREASED DNA METHYLATION 1 (ddm1) and DNA METHYLTRANSFERASE 1 (met1) mutants, as well as in the vegetative nucleus of pollen grains and in dedifferentiated plant cell cultures. Here we show that easiRNAs in Arabidopsis thaliana resemble secondary siRNAs, in that thousands of transposon transcripts are specifically targeted by more than 50 miRNAs for cleavage and processing by RDR6. Loss of RDR6, DCL4 or DCL1 in a ddm1 background results in loss of 21-nucleotide easiRNAs and severe infertility, but 24-nucleotide hetsiRNAs are partially restored, supporting an antagonistic relationship between PTGS and TGS. Thus miRNA-directed easiRNA biogenesis is a latent mechanism that specifically targets transposon transcripts, but only when they are epigenetically reactivated during reprogramming of the germ line. This ancient recognition mechanism may have been retained both by transposons to evade long-term heterochromatic silencing and by their hosts for genome defence.
authors.affiliation: Cold Spring Harbor Laboratory, 1 Bungtown Road, Cold Spring Harbor, New York 11724, USA.
authors.forename: Kate M
authors.initials: KM
authors.lastname: Creasey
authors.affiliation: Delaware Biotechnology Institute and Department of Plant & Soil Sciences, 15 Innovation Way, University of Delaware, Newark, Delaware 19711, USA.
authors.forename: Jixian
authors.initials: J
authors.lastname: Zhai
authors.affiliation: Cold Spring Harbor Laboratory, 1 Bungtown Road, Cold Spring Harbor, New York 11724, USA.
authors.forename: Filipe
authors.initials: F
authors.lastname: Borges
authors.affiliation: Cold Spring Harbor Laboratory, 1 Bungtown Road, Cold Spring Harbor, New York 11724, USA.
authors.forename: Frederic
authors.initials: F
authors.lastname: Van Ex
authors.affiliation: Cold Spring Harbor Laboratory, 1 Bungtown Road, Cold Spring Harbor, New York 11724, USA.
authors.forename: Michael
authors.initials: M
authors.lastname: Regulski
authors.affiliation: Delaware Biotechnology Institute and Department of Plant & Soil Sciences, 15 Innovation Way, University of Delaware, Newark, Delaware 19711, USA.
authors.forename: Blake C
authors.initials: BC
authors.lastname: Meyers
authors.affiliation: 1] Cold Spring Harbor Laboratory, 1 Bungtown Road, Cold Spring Harbor, New York 11724, USA [2] Howard Hughes Medical Institute-Gordon and Betty Moore Foundation, Cold Spring Harbor Laboratory, New York 11724, USA [3] Chaire Blaise Pascal, Institut de Biologie de l'Ecole Normale Supérieure (IBENS), 75230 Paris, France.
authors.forename: Robert A
authors.initials: RA
authors.lastname: Martienssen
mesh_terms: D017360:Arabidopsis / Q000235:genetics*; D001483:Base Sequence; D017124:Conserved Sequence; D004251:DNA Transposable Elements / Q000235:genetics; D044127:Epigenesis, Genetic; D018745:Genome, Plant / Q000235:genetics; D035683:MicroRNAs / Q000235:genetics* / Q000378:metabolism; D008957:Models, Genetic; D016366:Open Reading Frames / Q000235:genetics; D034741:RNA, Small Interfering / Q000096:biosynthesis / Q000235:genetics*; D018626:Retroelements / Q000235:genetics*
chemical_list: D004251:DNA Transposable Elements; D035683:MicroRNAs; D034741:RNA, Small Interfering; D018626:Retroelements