Phased Small RNAs in Plants: Novel Roles for Secondary siRNAs

The animal germline specifically expresses PIWI-interacting RNAs (piRNAs) that contribute to epigenetic reprogramming, transposon inactivation, and germline development. Although highly abundant in most metozoans, the plant germline lacks piRNAs.  However, analysis of maize and rice anthers has identified two novel classes of highly abundant small RNAs. We used developmentally staged anthers to show that one class of phased, secondary siRNAs (‘phasiRNAs’) emerges abruptly in pre-meiotic stages during cell fate specification. A second class, generated by a specialized, monocot-specific DICER, emerges coordinately with germinal cell maturation and meiosis, persisting into mature pollen. Male-sterile mutants distinguish these classes and demonstrate that there are distinct regulatory features of these small RNAs, both spatially and temporally. Thus the grasses contain analogs of animal piRNAs: one class of small RNAs participating in pre-meiotic development and a second related to meiosis. While differences in their biogenesis indicate their independent origins, grass phasiRNAs and mammalian piRNAs share characteristics such as developmental timing, genomic distribution, unique non-coding precursors and the sterility of mutants, suggesting an evolutionary convergence of reliance on small RNAs and their essential roles in male reproduction in both plants and animals.