Plant 24-nt reproductive phasiRNAs from intramolecular duplex mRNAs in diverse monocots
- Atul Kakrana1,2,
- Sandra M. Mathioni3,
- Kun Huang2,
- Reza Hammond1,2,
- Lee Vandivier4,
- Parth Patel1,2,
- Siwaret Arikit5,
- Olga Shevchenko2,
- Alex E. Harkess3,
- Bruce Kingham2,
- Brian D. Gregory4,
- James H. Leebens-Mack6 and
- Blake C. Meyers3,7
- 1Center for Bioinformatics and Computational Biology, University of Delaware, Newark, Delaware 19714, USA;
- 2Delaware Biotechnology Institute, University of Delaware, Newark, Delaware 19711, USA;
- 3Donald Danforth Plant Science Center, St. Louis, Missouri 63132, USA;
- 4Department of Biology, University of Pennsylvania, Philadelphia, Pennsylvania 19104, USA;
- 5Department of Agronomy, Faculty of Agriculture at Kamphaeng Saen and Rice Science Center, Kasetsart University, Kamphaeng Saen, Nakhon Pathom 73140, Thailand;
- 6Department of Plant Biology, University of Georgia, Athens, Georgia 30602, USA;
- 7Division of Plant Sciences, University of Missouri, Columbia, Missouri 65211, USA
Abstract
In grasses, two pathways that generate diverse and numerous 21-nt (premeiotic) and 24-nt (meiotic) phased siRNAs are highly enriched in anthers, the male reproductive organs. These “phasiRNAs” are analogous to mammalian piRNAs, yet their functions and evolutionary origins remain largely unknown. The 24-nt meiotic phasiRNAs have only been described in grasses, wherein their biogenesis is dependent on a specialized Dicer (DCL5). To assess how evolution gave rise to this pathway, we examined reproductive phasiRNA pathways in nongrass monocots: garden asparagus, daylily, and lily. The common ancestors of these species diverged approximately 115–117 million years ago (MYA). We found that premeiotic 21-nt and meiotic 24-nt phasiRNAs were abundant in all three species and displayed spatial localization and temporal dynamics similar to grasses. The miR2275-triggered pathway was also present, yielding 24-nt reproductive phasiRNAs, and thus originated more than 117 MYA. In asparagus, unlike in grasses, these siRNAs are largely derived from inverted repeats (IRs); analyses in lily identified thousands of precursor loci, and many were also predicted to form foldback substrates for Dicer processing. Additionally, reproductive phasiRNAs were present in female reproductive organs and thus may function in both male and female germinal development. These data describe several distinct mechanisms of production for 24-nt meiotic phasiRNAs and provide new insights into the evolution of reproductive phasiRNA pathways in monocots.
Footnotes
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[Supplemental material is available for this article.]
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Article published online before print. Article, supplemental material, and publication date are at http://www.genome.org/cgi/doi/10.1101/gr.228163.117.
- Received July 23, 2017.
- Accepted July 11, 2018.
This article is distributed exclusively by Cold Spring Harbor Laboratory Press for the first six months after the full-issue publication date (see http://genome.cshlp.org/site/misc/terms.xhtml). After six months, it is available under a Creative Commons License (Attribution-NonCommercial 4.0 International), as described at http://creativecommons.org/licenses/by-nc/4.0/.
