miR2118-dependent U-rich phasiRNA production in rice anther wall development

Araki, Saori; Le, Ngoc Tu; Koizumi, Koji; Villar‐Briones, Alejandro; Nonomura, Ken‐Ichi; Endo, Masaki; Inoue, Haruhiko; Saze, Hidetoshi; Komiya, Reina

doi:10.1038/s41467-020-16637-3

Cited by 73 publications

(50 citation statements)

References 51 publications

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“…We also observed strong differences in the nucleotide composition of the 5' end of phasiRNAs, mainly for 21-nt phasiRNAs, depending on the library construction method. This type of bias has been observed previously in sequencing data (30,33), and attributed to a preference of an Argonaute -that is, a relevant biological bias. However, our results suggest that this bias might also be technical in nature, influenced by the library construction method.…”

Section: Discussionsupporting

confidence: 72%

Ligation bias is a major contributor to nonstoichiometric abundances of secondary siRNAs and impacts analyses of microRNAs

Baldrich

Tamim

Mathioni

2020

Preprint

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Plant small RNAs are a diverse and complex set of molecules, ranging in length from 21 to 24 nt, involved in a wide range of essential biological processes. High-throughput sequencing is used for the discovery and quantification of small RNAs. However, several biases can occur during the preparation of small RNA libraries, especially using low input RNA. We used two stages of maize anthers to evaluate the performance of seven commercially-available methods for small RNA library construction, using different RNA input amounts. We show that when working with plant material, library construction methods have differing capabilities to capture small RNAs, and that different library construction methods provide better results when applied to the detection of microRNAs, phasiRNAs, or tRNA-derived fragment. We also observed that ligation bias occurs at both ends of miRNAs and phasiRNAs, suggesting that the biased compositions observed in small RNA populations, including nonstoichiometric levels of phasiRNAs within a locus, may reflect a combination of biological and technical influences.

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Section: Discussionsupporting

confidence: 72%

Ligation bias is a major contributor to nonstoichiometric abundances of secondary siRNAs and impacts analyses of microRNAs

Baldrich

Tamim

Mathioni

2020

Preprint

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“…Notably, a group of 21-nucleotide (nt) phased secondary siRNAs (phasiRNAs) were reported to exhibit a burst of expression in grass inflorescences from the premeiosis stage and to decrease in expression at the end of meiosis, when extensive gene expression changes occur [2][3][4][5][6][7][8] . These phasiRNAs are processed from precursors that contain miR2118-binding sites and might be triggered by miR2118 2,9 . More importantly, a differential accumulation of phasiRNAs is associated with photoperiod-sensitive male sterility in rice 10 .…”

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confidence: 99%

Reproductive phasiRNAs regulate reprogramming of gene expression and meiotic progression in rice

et al. 2020

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Plant spermatogenesis is a complex process that directly affects crop breeding. A rapid change in gene abundance occurs at early meiosis prophase, when gene regulation is selective. However, how these genes are regulated remains unknown. Here, we show that rice reproductive phasiRNAs are essential for the elimination of a specific set of RNAs during meiotic prophase I. These phasiRNAs cleave target mRNAs in a regulatory manner such that one phasiRNA can target more than one gene, and/or a single gene can be targeted by more than one phasiRNA to efficiently silence target genes. Our investigation of phasiRNA-knockdown and PHAS-edited transgenic plants demonstrates that phasiRNAs and their nucleotide variations are required for meiosis progression and fertility. This study highlights the importance of reproductive phasiRNAs for the reprogramming of gene expression during meiotic progression and establishes a basis for future studies on the roles of phasiRNAs with a goal of crop improvement.

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“…Defects in DCL5, which produces 24-nt phasiRNAs, lead to abnormalities of tapetum and temperature-sensitive male sterility in maize [16]. More recently, deletion of the miR2118 cluster in rice chromosome 4, which contains 14 MIR2118 loci (MIR2118b-MIR2118n), was demonstrated to cause severe defects in the development and morphology of somatic anther cell walls, and as a result, male and female sterility was observed for these rice mutants, revealing the biological significance of miR2118 and 21-nt phasiRNAs in rice reproduction [65]. However, mechanisms underlying the roles of phasiRNAs in male fertility remain elusive.…”

Section: Discussionmentioning

confidence: 99%

Widespread occurrence of microRNA-mediated target cleavage on membrane-bound polysomes

et al. 2021

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Background Small RNAs (sRNAs) including microRNAs (miRNAs) and small interfering RNAs (siRNAs) serve as core players in gene silencing at transcriptional and post-transcriptional levels in plants, but their subcellular localization has not yet been well studied, thus limiting our mechanistic understanding of sRNA action. Results We investigate the cytoplasmic partitioning of sRNAs and their targets globally in maize (Zea mays, inbred line “B73”) and rice (Oryza sativa, cv. “Nipponbare”) by high-throughput sequencing of polysome-associated sRNAs and 3′ cleavage fragments, and find that both miRNAs and a subset of 21-nucleotide (nt)/22-nt siRNAs are enriched on membrane-bound polysomes (MBPs) relative to total polysomes (TPs) across different tissues. Most of the siRNAs are generated from transposable elements (TEs), and retrotransposons positively contributed to MBP overaccumulation of 22-nt TE-derived siRNAs (TE-siRNAs) as opposed to DNA transposons. Widespread occurrence of miRNA-mediated target cleavage is observed on MBPs, and a large proportion of these cleavage events are MBP-unique. Reproductive 21PHAS (21-nt phasiRNA-generating) and 24PHAS (24-nt phasiRNA-generating) precursors, which were commonly considered as noncoding RNAs, are bound by polysomes, and high-frequency cleavage of 21PHAS precursors by miR2118 and 24PHAS precursors by miR2275 is further detected on MBPs. Reproductive 21-nt phasiRNAs are enriched on MBPs as opposed to TPs, whereas 24-nt phasiRNAs are nearly completely devoid of polysome occupancy. Conclusions MBP overaccumulation is a conserved pattern for cytoplasmic partitioning of sRNAs, and endoplasmic reticulum (ER)-bound ribosomes function as an independent regulatory layer for miRNA-induced gene silencing and reproductive phasiRNA biosynthesis in maize and rice.

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miR2118-dependent U-rich phasiRNA production in rice anther wall development

Cited by 73 publications

References 51 publications

Ligation bias is a major contributor to nonstoichiometric abundances of secondary siRNAs and impacts analyses of microRNAs

Ligation bias is a major contributor to nonstoichiometric abundances of secondary siRNAs and impacts analyses of microRNAs

Reproductive phasiRNAs regulate reprogramming of gene expression and meiotic progression in rice

Widespread occurrence of microRNA-mediated target cleavage on membrane-bound polysomes

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