24-nt reproductive phasiRNAs are broadly present in angiosperms

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.

sRNAanno --- a database repository of uniformly-annotated small RNAs in plants

“…2A). As reported before, 24- PHAS are more widely existed in monocots, but dispersed in eudicots without noticeable pattern ((Xia et al, 2019), Fig. 2A)…”

“…Therefore, we performed exhaustive PHAS profiling for the 138 plant species with at least one sequenced sRNA library. We used a well-developed p-value-based protocol to perform PHAS analysis ((Xia et al, 2013, 2019), Fig. S4).…”

“…To achieve a high confidence for miRNA annotation, we applied a set of uniform criteria adopted from the recently updated rules for plant miRNA annotation (Axtell and Meyers, 2018). For phasiRNA annotation, a p-value based approach established by our group was used for annotation of loci generating 21-nt phasiRNAs (21- PHAS ) or 24-nt phasiRNAs (24- PHAS ) (Xia et al, 2015, 2019). We also developed an algorithm based on sequence repetitiveness for the accurate annotation of loci generating hc-siRNAs, given their primary feature of generation from repetitive genomic regions.…”

Functional role of Polymerase IV during pollen development inCapsella

“…Biogenesis of premeiotic and meiotic phasiRNAs in maize seems to occur in the tapetum, rather than in meiocytes where they accumulate (Zhai et al, 2015b). The production of 24-nt phasiRNAs depends on miR2275, a pathway that is widely present in the eudicots, but missing in the Brassicaceae (Xia et al, 2019), suggesting evolutionary divergence of the functional role of phasiRNAs during pollen development. Cross-sections did not reveal obvious tapetal defects in Cr nrpd1, indicating that microspore arrest in Cr nrpd1 is not a consequence of a tapetal defect.…”

Reprogramming of 24nt siRNAs in rice gametes

“…2). 24nt phasiRNAs are expressed in meiotic anthers in diverse angiosperms including rice (Johnson et al 2009;Zhai et al 2015b;Xia et al 2019). In female reproductive tissues, phasiRNAs are not well characterized, but an argonaute called MEL1 that binds 21nt phasiRNAs is required for both male and female meiosis (Nonomura et al 2007;Komiya et al 2014).…”