Abstract
Small RNAs are key regulators in plant growth and development. One subclass, phased siRNAs (phasiRNAs) require a trigger microRNA for their biogenesis. In grasses, two pathways yield abundant phasiRNAs during anther development; miR2275 triggers one class, 24-nt phasiRNAs, coincident with meiosis, while a second class of 21-nt phasiRNAs are present in premeiotic anthers. Here we report that the 24-nt phasiRNA pathway is widely present in flowering plants, indicating that 24-nt reproductive phasiRNAs likely originated with the evolutionary emergence of anthers. Deep comparative genomic analyses demonstrated that this miR2275/24-nt phasiRNA pathway is widely present in eudicots plants, however, it is absent in legumes and in the model plant Arabidopsis, demonstrating a dynamic evolutionary history of this pathway. In Solanaceae species, 24-nt phasiRNAs were observed, but the miR2275 trigger is missing and some loci displaying 12-nt phasing. Both the miR2275-triggered and Solanaceae 24-nt phasiRNAs are enriched in meiotic stages, implicating these phasiRNAs in anther and/or pollen development, a spatiotemporal pattern consistent in all angiosperm lineages that deploy them.
Highlights
Small RNAs are key regulators in plant growth and development
We conclude that 24-nt phasiRNAs emerged in angiosperms, but were lost in some lineages, presumably reflecting life history adaptations
escape from adaptive conflict” (EAC) was invoked as an explanation for the expansion of RNA polymerases in plants[15], including Pol IV subunits that make DCL3 substrates for hc-siRNAs
Summary
Small RNAs are key regulators in plant growth and development. One subclass, phased siRNAs (phasiRNAs) require a trigger microRNA for their biogenesis. Phased secondary siRNAs or “phasiRNAs” in plants play key regulatory roles in growth, development, stress responses, and of importance to this work, in reproduction[1,2,3,4] They are typically triggered by a 22-nt microRNA (miRNA) directing Argonaute-mediated slicing of the primary precursor (“PHAS”) transcript, leading to recruitment of enzymes that make the sliced mRNA double-stranded and sequentially process it by a Dicer-like (DCL) protein into 21- or 24-nt siRNAs. In rice and maize, hundreds of loci on all chromosomes yield abundant 21-nt phasiRNAs in premeiotic anthers[4,5,6] and 24-nt phasiRNAs enriched in meiotic-stage anthers[4,5]. We report that this pathway is widely present in eudicots, consistent with an important role in flowering plant reproductive biology
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