Abstract
In grasses, phased small interfering RNAs (phasiRNAs), 21- or 24-nucleotide (nt) in length, are predominantly expressed in anthers and play a role in regulating male fertility. However, their targets and mode of action on the targets remain unknown. Here we profile phasiRNA expression in premeiotic and meiotic spikelets as well as in purified male meiocytes at early prophase I, tetrads and microspores in rice. We show that 21-nt phasiRNAs are most abundant in meiocytes at early prophase I while 24-nt phasiRNAs are more abundant in tetrads and microspores. By performing highly sensitive degradome sequencing, we find that 21-nt phasiRNAs direct target mRNA cleavage in male germ cells, especially in meiocytes at early prophase I. These targets include 435 protein-coding genes and 71 transposons that show an enrichment for carbohydrate biosynthetic and metabolic pathways. Our study provides strong evidence that 21-nt phasiRNAs act in a target-cleavage mode and may facilitate the progression of meiosis by fine-tuning carbohydrate biosynthesis and metabolism in male germ cells.
Highlights
In grasses, phased small interfering RNAs, 21- or 24-nucleotide in length, are predominantly expressed in anthers and play a role in regulating male fertility
The cleavage products serve as templates for RNA-dependent RNA polymerase 6 (RDR6) to produce double-stranded RNAs15, which are processed into 21- and 24-nt phasiRNAs by DCL4 and DCL3b, respectively[9]
Pre-meiotic spikelets (Fig. 1a, v), in which anthers are at stage 2 to stage 3 (Fig. 1a, vi)[23], meiotic spikelets (Fig. 1a, vii), in which germ cells are mostly at the early prophase of meiosis I, and embryos from germinated seeds, were collected as controls
Summary
In grasses, phased small interfering RNAs (phasiRNAs), 21- or 24-nucleotide (nt) in length, are predominantly expressed in anthers and play a role in regulating male fertility. By performing highly sensitive degradome sequencing, we find that 21-nt phasiRNAs direct target mRNA cleavage in male germ cells, especially in meiocytes at early prophase I. These targets include 435 protein-coding genes and 71 transposons that show an enrichment for carbohydrate biosynthetic and metabolic pathways. 1234567890():,; In plants, small RNAs (sRNAs) including microRNAs (miRNAs) and small interfering RNAs (siRNAs) are produced by Dicer-like (DCL) proteins and are associated with Argonaute (AGO) family proteins They regulate target genes post-transcriptionally through cleaving mRNAs and repressing translation, or transcriptionally through directing DNA methylation[1–5]. Overaccumulation of 21-nt phasiRNAs derived from the photoperiod-sensitive genic male sterility 1 (Pms1) locus in rice causes photoperiod-sensitive male sterility[22] These findings suggest that phasiRNAs might play critical roles in regulating germ cell meiosis. We propose that 21-nt phasiRNAs regulate male germ cell development through fine-tuning the expression of a large group of genes that together contribute to the progression of meiosis
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